Ronald R. Hoy

Mechanically coupled ears for directional hearing in the parasitoid fly Ormia ochracea

An analysis is presented of the mechanical response to a sound field of the ears of the parasitoid fly Ormia ochracea. This animal shows a remarkable ability to detect the direction of an incident sound stimulus even though its acoustic sensory organs are in very close proximity to each other. This close proximity causes the arrival times of the sound pressures at the two ears to be less than 1 to 2 microseconds depending on the direction of propagation of the sound wave. The small differences in these two pressures must be processed by the animal in order to determine the incident direction of the sound. In this fly, the ears are so close together that they are actually joined by a cuticular structure which couples their motion mechanically and subsequently magnifies interaural differences. The use of a cuticular structure as a means to couple the ears to achieve directional sensitivity is novel and has not been reported in previous studies of directional hearing. An analytical model of the mechanical response of the ear to a sound stimulus is proposed which supports the claim that mechanical interaural coupling is the key to this animals ability to localize sound sources. Predicted results for sound fields having a range of incident directions are presented and are found to agree very well with measurements.

Categorical Perception of Sound Frequency by Crickets

Partitioning continuously varying stimuli into categories is a fundamental problem of perception. One solution to this problem, categorical perception, is known primarily from human speech, but also occurs in other modalities and in some mammals and birds. Categorical perception was tested in crickets by using two paradigms of human psychophysics, labeling and habituation-dishabituation. The results show that crickets divide sound frequency categorically between attractive (<16 kilohertz) and repulsive (>16 kilohertz) sounds. There is sharp discrimination between these categories but no discrimination between different frequencies of ultrasound. This demonstration of categorical perception in an invertebrate suggests that categorical perception may be a basic and widespread feature of sensory systems, from humans to invertebrates.

Harmonic Convergence in the Love Songs of the Dengue Vector Mosquito

The familiar buzz of flying mosquitoes is an important mating signal, with the fundamental frequency of the females flight tone signaling her presence. In the yellow fever and dengue vector Aedes aegypti, both sexes interact acoustically by shifting their flight tones to match, resulting in a courtship duet. Matching is made not at the fundamental frequency of 400 hertz (female) or 600 hertz (male) but at a shared harmonic of 1200 hertz, which exceeds the previously known upper limit of hearing in mosquitoes. Physiological recordings from Johnstons organ (the mosquitos “ear”) reveal sensitivity up to 2000 hertz, consistent with our observed courtship behavior. These findings revise widely accepted limits of acoustic behavior in mosquitoes.

Hyperacute directional hearing in a microscale auditory system.

The physics of sound propagation imposes fundamental constraints on sound localization: for a given frequency, the smaller the receiver, the smaller the available cues. Thus, the creation of nanoscale acoustic microphones with directional sensitivity is very difficult. The fly Ormia ochracea possesses an unusual ‘ear’ that largely overcomes these physical constraints; attempts to exploit principles derived from O. ochracea for improved hearing aids are now in progress. Here we report that O. ochracea can behaviourally localize a salient sound source with a precision equal to that of humans. Despite its small size and minuscule interaural cues, the fly localizes sound sources to within 2° azimuth. As the flys eardrums are less than 0.5 mm apart, localization cues are around 50 ns. Directional information is represented in the auditory system by the relative timing of receptor responses in the two ears. Low-jitter, phasic receptor responses are pooled to achieve hyperacute timecoding. These results demonstrate that nanoscale/microscale directional microphones patterned after O. ochracea have the potential for highly accurate directional sensitivity, independent of their size. Notably, in the fly itself this performance is dependent on a newly discovered set of specific coding strategies employed by the nervous system.

Agonistic behaviour in male and female field crickets, Gryllus bimaculatus, and how behavioural context influences its expression

Previous interactions with conspecifics influenced the pattern, frequency and intensity of agonistic behaviour in the field cricket Gryllus bimaculatus. Tactile contact appeared to be the most important sensory cue responsible for the observed shifts in behaviour. Contact with other adult males promoted the production of aggressive song both during and after fights between males. However, individually housed males and males with restricted contact with conspecifics (once per day for 5 days) produced their aggressive song only at the end of an agonistic encounter. These two patterns of agonistic behaviour may reflect alternate fighting strategies. Prior experience influences whether sensory cues from a conspecific will initate agonistic behaviour. After males lost a fight, they displayed no further agonistic behaviour for 10 min but then gradually recovered their agonistic behaviour within an hour. This may be an important mechanism in preventing losing males from re-engaging a more powerful rival. Females were much less likely than males to attack conspecifics when food was plentiful. When food was scarce, females fought more often, and more successfully, than males for the contested resource.

Temporal Pattern as a Cue for Species-Specific Calling Song Recognition in Crickets

Female crickets can recognize conspecific calling song from its temporal pattern alone. In Teleogryllus oceanicus, the song pattern consists of three classes of interpulse intervals arranged in a stereotyped sequence. Females recognize a model song in which the sequential order of intervals is random. This argues against the hypothesis that recognition results from matching auditory input to an internal template of the song.

Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible neural link to phonotactic behavior

Summary1.In the cricket,Teleogryllus oceanicns, an identified auditory interneuron, interneuron-1 (int-1), is described morphologically and physiologically (Figs. 1,2). There is one such neuron in each hemiganglion of the prothoracic ganglion. The medial dendrites of int-1 overlap part of the terminal field formed by the auditory afferent axons from the ear and int-1s axon ascends to the brain, terminating on the same (ipsilateral) side (Fig- 2).2.The neuron has a two-part frequency response characteristic: (1) its spontaneous activity is suppressed by low frequencies (3 to 8 kHz) at threshold-to-moderate intensities (Fig. 9 B), and (2) it is strongly excited at high frequencies, especially ultrasonic, from 15–100 kHz (Fig. 3).3.Int-1 produces more spikes per tone pulse (Fig. 4) and its reponse latency decreases (Fig. 5), with increasing levels of intensity when stimulated by ultrasound.4.Two-tone inhibition occurs in int-1. When a 30 kHz (normally excitatory) tone is combined with a 5 kHz tone (which suppresses spontaneous activity), the combination tone results in a diminished response, compared to the response to the excitatory tone alone (Fig. 6).5.The excitation of int-1 shows lateralization. Excitation is stronger in the neuron ipsilateral to the sound source, than in the contralateral int-1 (Fig. 9).6.Int-1 responds to electronically-generated pulse trains that simulate bat-echolocation signals. The neuron is responsive to a range of ultrasonic frequencies that are contained in the echolocation signals of insectivorous bats (Fig. 11).7.In light of its response characteristics, we speculate that int-1 plays a role in the detection of ultrasonic signals emitted in the crickets normal environment by hunting bats.

Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea.

Sound localization is a basic processing task of the auditory system. The directional detection of an incident sound impinging on the ears relies on two acoustic cues: interaural amplitude and interaural time differences. In small animals, with short interaural distances both amplitude and time cues can become very small, challenging the directional sensitivity of the auditory system. The ears of a parasitoid fly Ormia ochracea, are unusual in that both acoustic sensors are separated by only 520 μm and are contained within an undivided air-filled chamber. This anatomy results in minuscule differences in interaural time cues (ca. 2 μs) and no measurable difference in interaural intensity cues generated from an incident sound wave.The tympana of both ears are anatomically coupled by a cuticular bridge. This bridge also mechanically couples the tympanana, providing a basis for directional sensitivity. Using laser vibrometry, it is shown that the mechanical response of the tympanal membranes has a pronounced directional sensitivity. Interaural time and intensity differences in the mechanical response of the ears are significantly larger than those available in the acoustic field. The tympanal membranes vibrate with amplitude differences of about 12 dB and time differences on the order of 50 μs to sounds at 90° off the longitudinal body axis. The analysis of the deflection shapes of the tympanal vibrations shows that the interaural differences in the mechanical response are due to the dynamic properties of the tympanal system and reflect its intrinsic sensitivity to the direction of a sound source. Using probe microphones and extracellular recording techniques, we show that the primary auditory afferents encode sound direction with a time delay of about 300 μs. Our data point to a novel mechanism for directional hearing in O. ochracea based on intertympanal mechanical coupling, a process that amplifies small acoustic cues into interaural time and amplitude differences that can be reliably processed at the neural level. An intuitive description of the mechanism is proposed using a simple mechanical model in which the ears are coupled through a flexible lever.

Demonstration of the precedence effect in an insect

Field crickets are interesting models for study of auditory phenomena because they solve many of the same acoustic problems as humans, but with simpler nervous systems. Previous work in this lab and others has investigated sound localization, frequency and temporal pattern discrimination, habituation and dishabituation, and categorical perception. This paper demonstrates the precedence effect in crickets, using a standard two-pulse paradigm with a directional escape response to ultrasound. When two pulses of ultrasound are presented form opposite sides with a delay between, crickets respond only to the first pulse for delays of approximately 4 to 75 ms. For delays of 0 to 2 ms, the direction of response is variable (the first wave front does not have precedence); for delays over approximately 75 ms, crickets respond directionally to each of the two pulses. Some neural correlates of the precedence effect were studied by using this paradigm during recordings from a bilateral pair of ascending second-order auditory interneurons known to initiate ultrasound avoidance. There are no ipsilateral-contralateral differences in their responses that could account for the precedence effect; such interactions in the brain must be involved instead. This seems to be the first test of precedence effect in a nonmammal.

Phonotaxis in flying crickets

Summary1.The steering responses of three species of field crickets,Teleogryllus oceanicus, T. commodus, andGryllus bimaculatus, were characterized during tethered flight using single tonepulses (rather than model calling song) presented at carrier frequencies from 3–100 kHz. This range of frequencies encompasses the natural songs of crickets (4–20 kHz, Fig. 1) as well as the echolocation cries of insectivorous bats (12–100 kHz).2.The single-pulse stimulus paradigm was necessary to assess the aversive nature of high carrier frequencies without introducing complications due to the attractive properties of repeated pulse stimuli such as model calling songs. Unlike the natural calling song, single tone-pulses were not attractive and did not elicit positive phonotactic steering even when presented at the calling song carrier frequency (Figs. 2, 3, and 9). In addition to temporal pattern, phonotactic steering was sensitive to carrier frequency as well as sound intensity. Three discrete flight steering behaviors (1)positive phonotaxis, (2)negative phonotaxis and (3)evasion, were elicited by appropriate combinations of frequency, temporal pattern and sound intensity (Fig. 12). Positive phonotactic steering required a model calling song temporal pattern, was tuned to 5 kHz and was restricted to frequencies below 9 kHz. Negative phonotactic steering, similar to the ‘early warning’ bat-avoidance behavior of moths, was produced by low intensity (55 dB SPL) tone-pulses at frequencies between 12 and 100 kHz (Figs. 2, 3, and 9). In contrast to model calling song, single tone-pulses of high intensity 5–10 kHz elicited negative phonotactic steering; low intensity ultrasound (20–100 kHz) produced only negative phonotactic steering, regardless of pulse repetition pattern. ‘Evasive’, side-to-side steering, similar to the ‘last-chance’ bat-evasion behavior of moths was produced in response to high intensity (> 90 dB) ultrasound (20–100 kHz).3.Since the demonstration of negative phonotactic steering did not require the use of a calling song temporal pattern, avoidance of ultrasound cannot be the result of systematic errors in localizing an inherently attractive stimulus when presented at high carrier frequencies. Unlike attraction to model calling song, the ultrasound-mediated steering responses were of short latency (25–35 ms) and were produced in an open loop manner (Fig. 4), both properties of escape behaviors. The ultrasound-mediated steering behaviors were produced in response to a variety of synthetic acoustic stimuli resembling bat biosonar, e.g. short ultrasonic pulses (as short as 1 ms), repetition rates from 1–500 pps and frequencies from 15 to 100 kHz (Figs. 5, 6), and were strikingly similar to the bat-escape behaviors of moths.4.Like moths, flying crickets steered away from low intensity ultrasound indicative of distant bats (10–18 m away), but produced the ‘evasive’ steering in response to high intensity ultrasound indicative of a closely approaching bat at 1–2 m. Theoretical calculations of ultrasound transmission predict that crickets can detect and avoid ultrasound at distances on the order of tens of meters, well beyond the detection abilities of bats for insect-size objects (less than 5 m) (Fig. 11). The ultrasound-mediated steering behavior of flying crickets is well suited to bat-avoidance. This study demonstrates that acoustically mediated steering in flying crickets is more diverse and more complex than previously thought.